Programmed genome rearrangements in ciliates
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Cellular and Molecular Life Sciences
REVIEW
Programmed genome rearrangements in ciliates Iwona Rzeszutek1 · Xyrus X. Maurer‑Alcalá2 · Mariusz Nowacki2 Received: 6 January 2020 / Revised: 11 May 2020 / Accepted: 15 May 2020 © The Author(s) 2020
Abstract Ciliates are a highly divergent group of unicellular eukaryotes with separate somatic and germline genomes found in distinct dimorphic nuclei. This characteristic feature is tightly linked to extremely laborious developmentally regulated genome rearrangements in the development of a new somatic genome/nuclei following sex. The transformation from germline to soma genome involves massive DNA elimination mediated by non-coding RNAs, chromosome fragmentation, as well as DNA amplification. In this review, we discuss the similarities and differences in the genome reorganization processes of the model ciliates Paramecium and Tetrahymena (class Oligohymenophorea), and the distantly related Euplotes, Stylonychia, and Oxytricha (class Spirotrichea). Keywords Ciliates · Nuclear dimorphism · Genome rearrangement · DNA elimination · Small non-coding RNAs
Introduction Developmentally regulated genome rearrangements (DRGRs) involve the elimination of specific DNA sequences (from the germline) somatic cell lineages. In most cases, this phenomenon is associated with two forms of DNA elimination either: (a) chromosome elimination where the entire chromosome is lost [1] or (b) chromosome diminution, a process characterized by loss of chromosome portions through chromosome breakage and repair during the developmental transformation from germline to soma [2, 3]. Programmed DNA elimination was first described in 1887 by Theodor Boveri [4] in the horse parasitic nematode, Parascaris univalens. Since then, DRGRs have been identified in diverse multicellular organisms including nematodes, arthropods, hagfish, lampreys [3] and lymphoid lineages of vertebrates [5]. However, it appears most pervasive in ciliates, an ancient clade of microbial eukaryotes (> 1 Gya; [6]), * Iwona Rzeszutek [email protected] * Mariusz Nowacki [email protected] 1
Institute of Biology and Biotechnology, Department of Biotechnology, University of Rzeszow, Pigonia 1, 35‑310 Rzeszow, Poland
Institute of Cell Biology, University of Bern, Baltzerstrasse 4, 3012 Bern, Switzerland
2
where genome rearrangements lead to the elimination of 30–95% of the germline genome [7–9]. This review will focus on genome rearrangements in the two best-studied classes of ciliates: the Oligohymenophorea (including Paramecium and Tetrahymena), and members of the Spirotrichea (including Euplotes, Oxytricha and Stylonychia).
Ciliates as a model organism Ciliates are unicellular eukaryotes found in diverse environments (fresh/saltwater as well as soil) across the globe that emerged more than 1 billion years ago [6]. Due to their morphological and morphogenetic characters, the taxonomy of ciliates has been ambiguous for a long time. Numerous studies have improved the phylogenetic relationship between ciliat
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